The integration of sensory feedback in the modulation of anuran landing preparation

Abstract

Controlled landing requires preparation. Mammals and bipedal birds vary how they prepare for landing by predicting the timing and magnitude of impact from the integration of visual and non-visual information. Here we explore how an animal that moves primarily through hopping, Rhinella marina, the cane toad, integrates sensory information to modulate landing preparation. Earlier work suggests toads may modulate landing preparation using predictions of impact timing and/or magnitude based on non-visual sensory feedback during takeoff rather than visual cues about the landing itself. Here we disentangled takeoff and landing conditions by hopping toads off platforms of different heights and measured electromyographic (EMG) activity of an elbow extensor, m. anconeus, and used high-speed motion capture to quantify whole body and forelimb kinematics to test how toads integrate visual and non-visual information in landing preparation. We asked two questions: 1) when they conflict, do toads correlate landing preparation with takeoff or landing conditions? And 2) for hops with the same takeoff conditions, does visual information alter the timing of landing preparation? We found that takeoff conditions are a better predictor of the onset of landing preparation than landing conditions, but that visual information is not ignored. When hopping off higher platforms, toads start to prepare for landing later when takeoff conditions are invariant. This suggests that, unlike mammals, toads prioritize non-visual sensory feedback about takeoff conditions to coordinate landing, but that they do integrate visual information to fine-tune landing preparation.

Hindlimb muscle spindles inform preparatory forelimb coordination prior to landing in toads

“…6 B). Additionally, the onset of anconeus activation during the aerial phase in the post-reinnervation condition was significantly delayed – occurring closer to hindlimb take-off – compared with values reported in Cox and Gillis (2020) (one-sample t -test, P <0.0001) and from Cox et al (2018) (one-sample t -test, P <0.0001; Fig. 6 C).…”

“…We also showed a significant reduction in the duration of anconeus (elbow extensor) activation during the aerial phase in toads 6 months post-reinnervation compared with the intact toads from Cox et al (2018) (one-sample t -test, P <0.0001) and Cox and Gillis (2020) (one-sample t -test, P <0.0001; Fig. 6 B).…”

“…(A) The duration of plantaris ( N =6; 91 jumps) activity prior to take-off, (B) the duration of anconeus ( N =6; 187 jumps) activation during the aerial phase, and (C) the onset time of the anconeus ( N =6; 187 jumps) following hindlimb take-off. Data are from the present study, Gillis and Biewener (2000) , Cox et al (2018) and Cox and Gillis (2020) . Clouds and small circles to the right of the same color represent the distribution and all jumps recorded, respectively.…”

Semicircular canal size constrains vestibular function in miniaturized frogs

“…This too is consistent with our observations of Brachycephalus (movies S2 to S6). Forelimb movement in the absence of vestibular feedback indicates control via a nonvestibular mechanism ( 16 , 21 , 22 ), possibly as a reflexive response driven by proprioception resulting from hindlimb extension at the launch ( 22 ).…”

Cooperation behavior of fore‐ And hindlimbs during jumping in Rana dybowskii and Xenopus laevis

“…Fore-and hindlimbs, function, kinematics, Rana dybowskii, short jump, Xenopus laevis Generally, frogs' jump can be divided into four phases: preparation, takeoff, flight, and landing. The first phase begins with a crouched stationary position, preparing for the takeoff phase; the takeoff phase of jumping involves rapid hindlimbs extension accompanied by loss of forelimbs contact; the flight phase is characterized by midair body and limbs rotations in preparation for landing; landing begins when forelimbs or body touch the ground, and then, the flexed hindlimbs rotate into position beneath the body, enabling the rapid preparation of another takeoff (Azizi et al, 2014;Cox & Gillis., 2016, 2020. To escape from external danger optimally, all phases should be in short duration.…”